Abstract
The effects of ultraviolet (UV) irradiation (up to 0.6 J/cm2) and heating (65 °C, 20 min) on the absorption spectra and electron transfer in dehydrated film samples of photosynthetic reaction centers (RCs) from purple bacterium Rhodobacter (Rb.) sphaeroides, as well as in hybrid structures consisting of RCs and quantum dots (QDs), have been studied. The samples were placed in organic matrices containing the stabilizers of protein structure—polyvinyl alcohol (PVA) and trehalose. UV irradiation led to partially irreversible oxidation of some RCs, as well as to transformation of some fraction of the bacteriochlorophyll (BChl) molecules into bacteriopheophytin (BPheo) molecules. In addition, UV irradiation causes degradation of some BChl molecules that is accompanied by formation of 3-acetyl-chlorophyll a molecules. Finally, UV irradiation destroys the RCs carotenoid molecules. The incorporation of RCs into organic matrices reduced pheophytinization. Trehalose was especially efficient in reducing the damage to the carotenoid and BChl molecules caused by UV irradiation. Hybrid films containing RC + QD were more stable to pheophytinization upon UV irradiation. However, the presence of QDs in films did not affect the processes of carotenoid destruction. The efficiency of the electronic excitation energy transfer from QD to P865 also did not change under UV irradiation. Heating led to dramatic destruction of the RCs structure and bacteriochlorins acquired the properties of unbound molecules. Trehalose provided strong protection against destruction of the RCs and hybrid (RC + QD) complexes.
Similar content being viewed by others
Abbreviations
- RC:
-
Reaction center
- QD:
-
Quantum dot
- BChl:
-
Bacteriochlorophyll
- BPheo:
-
Bacteriopheophytin
- P865:
-
Photoactive dimer of BChl
- UV:
-
Ultraviolet
- PVA:
-
Polyvinyl alcohol
- P865+ :
-
Photooxidized dimer of BChl
- Q A and Q B :
-
Primary and secondary quinone acceptors
- Rb. sphaeroides :
-
Purple bacteria Rhodobacter sphaeroides
References
Allakhverdiev SI, Hayashi H, Nishiyama Y, Ivanov AG, Aliev JA, Klimov VV, Murata N, Carpentier R (2003) Glycinebetaine protects the D1/D2/Cytb559 complex of photosystem II against photo-induced and heat-induced inactivation. J Plant Physiol 160:41–49
Čejková J, Čejka Č, Ardan T, Širc J, Michálek J, Luyckx J (2010) Reduced UVB-induced corneal damage caused by reactive oxygen and nitrogen species and decreased changes in corneal optics after trehalose treatment. Histol Histopathol 25:1403–1416
Chen G, Djuric Z (2001) Carotenoids are degraded by free radicals but do not affect lipid peroxidation in unilamellar liposomes under different oxygen tensions. FEBS Lett 505:151–154
Chen X, Li M, Li L, Xu S, Huang D, Ju M, Huang Y, Chen K, Gu H (2016) Trehalose, sucrose and raffinose are novel activators of autophagy in human keratinocytes through an mTOR-independent pathway. Sci Rep 6:28423
Clayton RK (1978) Effects of dehydration on reaction centers from Rps. sphaeroides. Biochim Biophys Acta 504:255–264
Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599
D’Alfonso L, Collini M, Cannone F, Chirico G, Campanini B, Cottone G, Cordone L (2007) GFP-mut2 proteins in trehalose-water matrixes: spatially heterogeneous protein-water-sugar structures. Biophys J 93:284–293
De Las Rivas J, Barber J (1997) Structure and thermal stability of photosystem II reaction centers studied by infrared spectroscopy. Biochemistry 36:8897–8903
Francia F, Palazzo G, Mallardic A, Cordoned L, Venturoli G (2004) Probing light-induced conformational transitions in bacterial photosynthetic reaction centers embedded in trehalose–water amorphous matrices. Biochim Biophys Acta 1658:50–57
Gast P, Hemelrijk PW, Van Gorkom HJ, Hoff AJ (1996) The association of different detergents with the photosynthetic reaction center protein of Rhodobacter sphaeroides R26 and the effects on its photochemistry. Eur J Biochem 239:805–809
Gingras G (1978) A comparative review of photochemical reaction center preparations from photosynthetic bacteria. In: Clayton RK, Sistrom WR (eds) The photosynthetic bacteria. Plenum Press, New York, pp 119–131
Giuffrida S, Cottone G, Cordone L (2004) Structure—dynamics coupling between protein and external matrix in sucrose-coated and in trehalose-coated MbCO: an FTIR study. J Phys Chem B 108:15415–15421
Hughes AV, Rees P, Heathcote P, Jones MR (2006) Kinetic analysis of the thermal stability of the photosynthetic reaction center from Rhodobacter sphaeroides. Biophys J 90:4155–4166
Ivanov AG, Miskiewicz E, Clarke AK, Greenberg BM, Huner NPA (2000) Protection of photosystem II against UV-A and UV-B-radiation in the cyanobacterium Plectonema boryanum: the role of growth temperature and growth irradiance. Photochem Photobiol 72:772–779
Karpulevich AA, Maksimov EG, Sluchanko NN, Vasiliev AN, Paschenko VZ (2016) Highly efficient energy transfer from quantum dot to allophycocyanin in hybrid structures. J Photochem Photobiol B 160:96–101
Karpulevich AA, Maksimov EG, Gorokhov VV, Churin AA, Ivanov MV, Paschenko VZ (2017) Covalently linked hybrid structures of semiconductor nanocrystals and allophycocyanin. Nanotechnol Russ 12:98–106
Knox PP, Kononenko AA, Rubin AB (1979) Functional activity in photosynthetic reaction centers from Rhodopseudomonas sphaeroides at fixed hydration levels of the preparations. Bioorganic Chem (USSR) 5:879–885
Knox PP, Lukashev EP, Timofeev KN, Seifullina NK (2002) Effects of oxygen on the dark recombination between photoreduced secondary quinone and oxidized bacteriochlorophyll in Rhodobacter sphaeroides reaction centers. Biochemistry 67:901–907
Konov KB, Isaev NP, Dzuba SA (2014) Low-temperature molecular motions in lipid bilayers in the presence of sugars: insights into cryoprotective mechanisms. J Phys Chem B 118:12478–12485
Kotakis C, Akhtar P, Zsiros O, Garab G, Lambrey PH (2018) Increased thermal stability of photosystem II and the macro-organization of thylakoid membranes, induced by co-solutes, associated with changes in the lipid-phase behaviour of thylakoid membranes. Photosynthetica 56:254–264
Lancaster CRD, Michel H, Honig B, Gunner MR (1996) Calculated coupling of electron and proton transfer in the photosynthetic reaction center of Rhodopseudomonas viridis. Biophys J 70:2469–2492
Leatherdale CA, Woo WK, Mikulec FV, Bawendi MG (2002) On the absorption cross section of CdSe nanocrystal quantum dots. J Phys Chem B 106:7619–7622
Lukashev EP, Knox PP, Gorokhov VV, Grishanova NP, Seifullina NK, Krikunova M, Lokstein H, Paschenko VZ (2016a) Purple bacterial photosynthetic reaction centers and quantum-dot hybrid-assemblies in lecithin liposomes and thin films. J Photochem Photobiol B 164:73–82
Lukashev EP, Knox PP, Oleinikov IP, Seifullina NK, Grishanova NP (2016b) Investigation of stability of photosynthetic reaction center and quantum dot hybrid films. Biochemistry 81:58–63
Makhneva ZK, Ashikhmin AA, Bolshakov MA, Moskalenko AA (2016) 3-Acetyl-chlorophyll formation in light-harvesting complexes of purple bacteria by chemical oxidation. Biochemistry 81:176–186
Maksimov EG, Gostev TS, Kuz’minov FI, Sluchanko NN, Stadnichuk IN, Pashchenko VZ, Rubin AB (2010) Hybrid systems of quantum dots mixed with the photosensitive protein phycoerythrin. Nanotechnol Russ 5:531–537
Malferrari M, Savitsky A, Mamedov MD, Milanovsky GE, Lubitz W, Möbius K, Semenov AY, Venturoli G (2016) Trehalose matrix effects on charge-recombination kinetics in рhotosystem I of oxygenic photosynthesis at different dehydration levels. Biochim Biophys Acta 1857:1440–1454
McConnell I, Li G, Brudvig GW (2010) Energy conversion in natural and artificial photosynthesis. Chem Biol 17:434–447
Miksovska J, Maroti P, Tandori J, Schiffer M, Hanson DK, Sebban P (1996) Distant electrostatic interactions modulate the free energy level of QA − in the photosynthetic reaction center. Biochemistry 35:15411–15417
Nabiev I, Rakovich A, Sukhanova A, Lukashev E, Zagidullin V, Paschenko V, Rakovich Y, Donegan J, Rubin A, Govorov A (2010) Fluorescent quantum dots as artificial antennas for enhanced light harvesting and energy transfer to photosynthetic reaction centers. Angew Chem Int Ed 49:7217–7221
Okamura MY, Feher G (1992) Proton transfer in reaction centers from photosynthetic bacteria. Annu Rev Biochem 61:861–896
Okamura MY, Paddock ML, Graige MS, Feher G (2000) Proton and electron transfer in bacterial reaction centers. Biochim Biophys Acta 1458:148–163
Oleynikov VA, Sukhanova AV, Nabiev IR (2007) Fluorescent semiconductor nanocrystals for biology and medicine. Russ Nanotechnol 2:160–173
Olsson C, Jansson H, Swenson J (2016) The role of trehalose for the stabilization of proteins. J Phys Chem B 120:4723–4731
Ormerod JG, Ormerod KS, Gest H (1961) Dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; Relationships with nitrogen metabolism. Arch Biochem Biophys 94:449–463
Palazzo G, Mallardi A, Hochkoeppler A, Cordone L, Venturoli G (2002) Electron transfer kinetics in photosynthetic reaction centers embedded in trehalose glasses: trapping of conformational substates at room temperature. Biophys J 82:558–568
Rabenstein B, Ullmann GM, Knapp EW (2000) Electron transfer between the quinones in the photosynthetic reaction center and its coupling to conformational changes. Biochemistry 39:10487–10496
Razjivin AP, Lukashev EP, Kompanets VO, Kozlovsky VS, Ashikhmin AA, Chekalin SV, Moskalenko AA, Paschenko VZ (2017) Excitation energy transfer from the bacteriochlorophyll Soret band to carotenoids in the LH2 light-harvesting complex from Ectothiorhodospira haloalkaliphila is negligible. Photosynth Res 133:289–295
Reed DW, Peters GA (1972) Characterization of the pigments in reaction center preparations from Rhodopseudomonas sphaeroides. J Biol Chem 247:7148–7152
Tandori J, Mate Z, Maroti P, Vass I (1996) Resistance of reaction centers from Rhodobacter sphaeroides against UV-B radiation. Effects on protein structure and electron transport. Photosynth Res 50:171–179
Tokaji Z, Tandori J, Maroti P (2002) Light- and redox-dependent thermal stability of the reaction center of the photosynthetic bacterium Rhodobacter sphaeroides. Photochem Photobiol 75:605–612
Uchoa AF, Knox PP, Turchielle R, Seifullina NK, Baptista MS (2008) Singlet oxygen generation in the reaction centers of Rhodobacter sphaeroides. Eur Biophys J 37:843–850
Vass I, Sass L, Spetea C, Bakou A, Ghanotakis DF, Petrouleas V (1996) UV-B-induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence. Impairment of donor and acceptor side components. Biochemistry 35:8964–8973
Williams W, Gounaris K (1992) Stabilisation of PS-II-mediated electron transport in oxygen-evolving PS II core preparations by the addition of compatible co-solutes. Biochim Biophys Acta 1100:92–97
Zacharie U, Lancaster CRD (2001) Proton uptake associated with the reduction of the primary quinone QA influences the binding site of the secondary quinone QB in Rhodopseudomonas viridis photosynthetic reaction centers. Biochim Biophys Acta 1505:280–290
Zagidullin VE, Lukashev EP, Knox PP, Seifullina NK, Sokolova OS, Pechnikova EV, Lokstein H, Paschenko VZ (2014) Properties of hybrid complexes composed of photosynthetic reaction centers from the purple bacterium Rhodobacter sphaeroides and quantum dots in lecithin liposomes. Biochemistry 79:1183–1191
Zakharova NI, Churbanova IY (2000) Methods for isolating reaction center preparations from purple photosynthetic bacteria. Biochemistry 65:181–193
Zhang G, Zhu B, Nakamura Y, Shimoishi Y, Murata Y (2008) Structure-dependent photodegradation of carotenoids accelerated by dimethyl tetrasulfide under UVA irradiation. Biosci Biotechnol Biochem 72:2176–2183
Zhang N, Liu F-F, Dong X-Y, Sun Y (2012) Molecular insight into the counteraction of trehalose on urea-induced protein denaturation using molecular dynamics simulation. J Phys Chem B 116:7040–7047
Acknowledgements
This study was supported by the Russian Foundation for Basic Research (Project No. 15-29-01167).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Knox, P.P., Lukashev, E.P., Gorokhov, V.V. et al. Hybrid complexes of photosynthetic reaction centers and quantum dots in various matrices: resistance to UV irradiation and heating. Photosynth Res 139, 295–305 (2019). https://doi.org/10.1007/s11120-018-0529-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-018-0529-5